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Invasive Congeners Are Unlikely to Hybridize with Native Hawaiian Bidens

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Invasive Congeners Are Unlikely to Hybridize with Native Hawaiian Bidens American Journal of Botany 100(6): 1221–1226. 2013. I NVASIVE CONGENERS ARE UNLIKELY TO HYBRIDIZE WITH NATIVE HAWAIIAN B IDENS (ASTERACEAE) 1 M ATTHEW L. KNOPE 2,6 , R ICHARD J. PENDER 3 , D ANIEL J. CRAWFORD 4 AND A NIA M . W IECZOREK 5 2 Department of Geological and Environmental Sciences, Stanford University, 385 Serra Mall, Stanford, California 94305 USA; 3 Botany Department, University of Hawaii at Manoa, 3190 Maile Way, Honolulu, Hawaii 96822 USA; 4 Department of Ecology and Evolutionary Biology, and the Biodiversity Institute, University of Kansas, Lawrence, Kansas 66045 USA; and 5 Department of Tropical Plant and Soil Sciences, University of Hawaii at Manoa, 3190 Maile Way, Honolulu, Hawaii 96822 USA • Premise of the study: Invasive plant species threaten native plants in multiple ways, one of which is genetic assimilation through hybridization. However, information regarding hybridization between related alien and native plant species is gener- ally lacking. In Hawaii, the invasive Central American species Bidens pilosa and Bidens alba have colonized natural areas and often grow alongside the native Hawaiian Bidens species, a clade representing an adaptive radiation of 27 endemic taxa, many of which are threatened or endangered. • Methods: To assess the risk of hybridization between introduced and native Hawaiian Bidens (which will readily hybridize with one another), we undertook crosses in cultivation between the invasive species and nine native Bidens taxa. • Key results: The majority of the crosses formed no viable seed. Although seed did mature in several of the crosses, morphologi- cal screening of the resulting seedlings indicated that they were the result of self-pollination. • Conclusions: This result suggests that B. alba and B. pilosa are incapable of hybridizing with these Hawaiian Bidens taxa. Further, we found that B. alba in Hawaii was self-compatible, despite self-incompatibility throughout its native range, and that the tetraploid species B. alba and the hexaploid species B. pilosa were cross-compatible, although pollen fertility was low. Key words: adaptive radiation; Bidens ; conservation; endangered species; endemic species; gene fl ow; introgression; invasive species; islands; threatened species. Biotic invasions are a major threat to native biodiversity could lead to extinction of the native species. Assimilation oc- throughout the world ( Mack et al., 2000 ; Cadotte et al., 2006 ; curs when highly fertile hybrids backcross to parental species, Lövei et al., 2012 ), and invasive plants are commonly cited potentially resulting in the loss of one or both of the parental as examples of alien species threatening native species (e.g., species through time. This risk is potentially heightened if the Kueffer et al., 2010 ; Young et al., 2010 ). There have recently native populations are small relative to the alien populations been extensive efforts to identify the traits (e.g., life history, ( Wendel and Percy, 1990 ; Haber, 1998 ; Daehler and Carino, breeding system, prior evolutionary history) that predict inva- 2001 ). In addition, hybrid offspring that suffer lower fi tness siveness (e.g., Lloret et al., 2005 ; Abe et al., 2011 ; Castro-Díez than either parent, through reduced vigor, fertility, or abortion et al., 2011 ; Kaiser-Bunbury et al., 2011 ) and the factors that of embryos, may adversely affect the native species, particu- account for differences in the invasiveness of species ( Kueffer larly in small populations due to gametic wastage and reduced et al., 2010 ). One of the many processes by which invasive spe- seed set ( Daehler and Carino, 2001 ). cies pose threats to native species is interspecifi c hybridization The Hawaiian Islands fl ora may be particularly susceptible to ( Levin et al., 1996 ; Daehler and Carino, 2001 ). If native species the adverse affects of hybridization with invasive species. Ap- are cross-compatible and interfertile with alien species, and the proximately 89% of the 956 fl owering plant species native to fi tness of the resulting hybrids is equal to or exceeds their par- the Hawaiian Islands are endemic ( Wagner et al., 1999 ) and ents in some habitats, genetic assimilation and competition hybridization with alien congeners is known to occur. For ex- ample, naturally occurring hybrids between native-alien Rubus 1 ( Randell et al., 1998 ) and native-alien Portulaca ( Kim and Carr, Manuscript received 12 January 2013; manuscript accepted 11 March 1990 ) and both natural and greenhouse hybrids between native- 2013. M.L.K. gratefully acknowledges T. Fukami for support and advice; alien Gossypium species ( Stephens, 1964; Dejoode and Wendel, W. Haines, S. Hinard, K. Kawakame, J. Knope, T. Kutynina, K. McMillen, 1992 ) have been documented in Hawaii. Daehler and Carino K. A. McMillen, D. Okamoto, H. Oppenheimer, and A. Yoshinaga for assis- (2001) estimate that a total of 59 genera, consisting of 176 native tance in the fi eld; and the Ecology, Evolution, and Conservation Biology fl owering plant species in Hawaii, are potentially threatened with program at the University of Hawaii and the Dept. of Biology at Stanford hybridization by alien congeners. University for fi nancial support. L. Kerr, A. Lehman, S. Lucas, C. Okazaki, One of the largest lineages of Hawaiian fl owering plants and S. Walsh provided assistance with growing plants and undertaking is in the genus Bidens (family Asteraceae or Compositae, tribe crosses at UH. R.J.P. gratefully acknowledges the fi nancial support provided Coreopsideae), including 19 species and eight subspecies en- by Fulbright New Zealand and the John R. Templin Scholarship. K. Sadler demic to Hawaii, resulting from a single colonization event assisted with cultivation of plants at KU. Lastly, we thank P. Feinberg for image preparation, and L. Castillo Nelis, L. Frishkoff, T. Fukami, and two ( Ganders et al., 2000 ; Knope et al., 2012 ). Despite their coloni- anonymous reviewers for comments. zation of the archipelago within the last ~3 million years ( Knope 6 Author for correspondence (e-mail: [email protected]) et al., 2012 ), more morphological and ecological diversity ex- ists in the Hawaiian lineage than in the remaining ~300 species doi:10.3732/ajb.1300018 of Bidens distributed over fi ve continents ( Ganders and Nagata, American Journal of Botany 100(6): 1221–1226, 2013 ; http://www.amjbot.org/ © 2013 Botanical Society of America 1221 1222 AMERICAN JOURNAL OF BOTANY [Vol. 100 1984 ; Crawford et al., 2009 ; and see Fig. 1 ). The Hawaiian taxa and Lim, 1970 ) and will readily hybridize with one another are considered to be one of the best examples of adaptive radia- ( Ganders and Nagata, 1984 ). The Bidens pilosa species com- tion in the Hawaiian fl ora ( Carr, 1987 , and nine taxa are cur- plex, which has a center of diversity in its native range in Mexico rently of conservation concern, including both threatened and ( Ballard, 1986 ), is an invasive species now common in Hawaii, endangered taxa ( Wagner et al., 1999 ). Given the great ecologi- as it is in subtropical and tropical regions worldwide ( IUCN cal diversity of the Hawaiian Bidens ( Ganders and Nagata, ISSG, 2011 ). This species has a high score on the Hawaiian 1984 ; Crawford et al., 2009 ), any threat to the Hawaiian taxa Weed Risk Assessment ( HI-WRA, 2011 ), which is based on would impact a disproportionately high level of biological di- approximately 50 attributes that characterize invasive spe- versity relative to the overall number of taxa in the genus. Two cies. Bidens pilosa is morphologically variable, but the com- widely distributed species, Bidens pilosa and Bidens alba , have mon weedy form, like the native Hawaiian Bidens species, is been introduced into Hawaii, and they occur as the sister group hexaploid with a chromosome number of n = 36 ( Ballard, 1986 ). in the same large clade as the native Hawaiian Bidens species The species is self-compatible and exhibits autonomous autog- ( Ganders et al., 2000 ; Kimball and Crawford, 2004 ; Knope et al., amy with high seed set ( Sun and Ganders, 1990 ; Grombone- 2012 ). The close phylogenetic relationship between the native Guaratini et al., 2004 ). Bidens alba , a species that is closely and alien Bidens species suggests the potential for hybridiza- related to B. pilosa ( Ballard, 1986 ; Ganders et al., 2000 ; Knope tion in Hawaii. et al., 2012 ), is also invasive in Hawaii, and like B. pilosa , can The native species grow from sea level to over 2200 m in be found growing side-by-side with native Hawaiian Bidens elevation and occur in habitats ranging from semideserts to rain- species ( Gillett, 1972 ). We have also encountered fi ve native forests ( Ganders and Nagata, 1984 ). About half of the Hawaiian Bidens taxa growing immediately adjacent to one or the other native taxa are gynodioecious (dimorphic breeding system in of the introduced Bidens species in various locations through- which female individuals coexist with hermaphroditic indi- out Hawaii (M. L. Knope and R. J. Pender, personal observa- viduals in populations), a form of sex expression not known tions). However, B. alba differs from B . pilosa in being tetraploid elsewhere in Bidens ( Sun and Ganders, 1986 ). The Hawaiian ( n = 24) and has previously been considered self-incompatible species are self-compatible and those that have been investi- ( Ballard, 1986 ). gated have a mixed mating system ( Ritland and Ganders 1985 ; The purpose of the current study was to determine whether Sun and Ganders, 1986 ). All of Hawaii’s native Bidens species experimental hybrids between native Hawaiian Bidens species are hexaploid with a gametic chromosome number of 36 ( Gillett and B. pilosa or B. alba could be synthesized and thus provide Fig. 1. Representative invasive and native Hawaiian Bidens taxa used in experimental crosses: (A) B. pilosa (Central American species now invasive in Hawaii) (photo credit: G. D. Carr); (B) B. alba (Central American species now invasive in Hawaii) (photo credit: J. C. Knope); (C) Hawaiian native B. torta with C. W. Morden in foreground for scale (photo credit: G. D. Carr); (D) Hawaiian native B.
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